American Journal of Epidemiology Advance Access originally published online on March 6, 2007
American Journal of Epidemiology 2007 165(10):1143-1153; doi:10.1093/aje/kwm017
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ORIGINAL CONTRIBUTIONS |
The Impact of Highly Active Antiretroviral Therapy on Non-AIDS-Defining Cancers among Adults with AIDS
1 Department of Medicine, University of California, San Francisco, CA
2 AIDS Office, San Francisco Department of Public Health, San Francisco, CA
3 California Cancer Registry, Public Health Institute, Sacramento, CA
4 Department of Epidemiology and Biostatistics, University of California, San Francisco, CA
Correspondence to Nancy A. Hessol, University of California San Francisco, Department of Medicine, 405 Irving Street, 2nd Floor, San Francisco, CA 94122 (e-mail: Nancy.Hessol{at}ucsf.edu).
Received for publication May 2, 2006. Accepted for publication November 8, 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Highly active antiretroviral therapy (HAART) has dramatically reduced the incidence of acquired immunodeficiency syndrome (AIDS) and increased AIDS survival time, but little is known about its impact on cancer. Data from adults in the San Francisco, California, AIDS surveillance registry were computer matched with the California Cancer Registry. Age-, sex-, and race-adjusted standardized incidence ratios (SIRs) were computed, and proportional hazards models evaluated the effect of HAART use on cancer incidence and cancer survival time. Among 14,210 adults with AIDS diagnosed in 1990–2000, 482 non-AIDS-defining cancers were diagnosed. Compared with rates for the general population, significantly increased cancer incidence rates were observed for anal (SIR = 13.4), Hodgkin's lymphoma (SIR = 11.5), liver (SIR = 3.6), oral cavity and pharynx (SIR = 2.6), respiratory (SIR = 2.6), leukemia (SIR = 2.4), skin melanoma (SIR = 2.4), and prostate (SIR = 1.7) cancers. Risk of liver cancer was lower with HAART use (relative hazard (RH) = 0.32). Risk of anal cancer increased after 1995 (RH = 2.9). Respiratory cancer (RH = 0.40) and Hodgkin's lymphoma (RH = 0.17) showed increased cancer survival time with HAART use, while anal cancer survival may have been slightly decreased (RH = 1.4). The impact of HAART on non-AIDS-defining cancer incidence rates and survival is not uniform, and the mechanism(s) responsible for these differences should be investigated further.
acquired immunodeficiency syndrome; antiretroviral therapy, highly active; HIV infections; incidence; neoplasms; survival
Abbreviations: AIDS, acquired immunodeficiency syndrome; HAART, highly active antiretroviral therapy; HIV, human immunodeficiency virus; RH, relative hazard; SEER, Surveillance, Epidemiology, and End Results; SIR, standardized incidence ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The introduction and widespread use of highly active antiretroviral therapy (HAART) in the mid-1990s has led to reduced acquired immunodeficiency syndrome (AIDS) morbidity and mortality among people with human immunodeficiency virus (HIV) infection (1–3). However, longer life expectancy may also lead to the development of diseases that require a long latency period, such as cancer. Under these conditions, it is important to closely monitor for emerging epidemiologic trends to accurately determine the risks of malignancy in this population. Implementation of appropriate cancer prevention, screening, and treatment recommendations requires a better understanding of the etiology, epidemiology, and natural history of AIDS and non-AIDS-defining malignancies.
People with HIV infection are at increased risk of cancer, and an estimated 30–40 percent will develop a malignancy at some point during their infection (4). As people with HIV live longer, especially with advances in antiretroviral therapies, more people are expected to develop malignancies, including cancers not currently associated with HIV or AIDS.
The effect of potent antiretroviral therapy on the full spectrum of HIV-related cancers is still unknown. If treatment for HIV succeeds at immune restoration, then the incidence of some cancers may decline or at least be delayed. However, the reduced morbidity due to HIV infection and longer life expectancy associated with HAART may provide the longer latency period necessary for the development of certain cancers, including those not previously identified as HIV related. It will thus be important to study cancer incidence data for HIV-infected persons over time to ascertain the true impact of HAART on these cancers.
In this investigation, we examined the impact of HAART on the incidence and survival time of non-AIDS-defining cancers among adults with AIDS.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Using the San Francisco, California, AIDS surveillance registry, we identified all adult AIDS cases (aged 16–86 years) whose AIDS was initially diagnosed between 1990 and 2000. The AIDS surveillance registry in San Francisco has been described previously (5). In brief, reporting activities included active and passive case ascertainment, and reporting was estimated to be 97 percent complete. Information on start date of antiretroviral therapy (including initiation prior to AIDS), type of therapy used, and CD4 test results was recorded from medical records at the time of initial AIDS case report and every 12–18 months thereafter for persons whose ongoing care occurred in San Francisco. HAART was defined according to 2004 US Department of Health and Human Services guidelines (6).
We matched the adult AIDS cases with cancer cases diagnosed between 1985 and 2002 in the California Cancer Registry. This statewide, population-based registry collects cancer incidence and mortality information for all cancers except basal and squamous cell skin and in situ cervical cancers. At the time of match, the California Cancer Registry database contained 100 percent of the expected number of cancers for diagnosis years 1985–2000, 97 percent for the year 2001, and 67 percent for the year 2002. Name, Social Security number, date of birth, sex, race, and date of death were used to match cases in the AIDS and cancer registries. To verify possible matches, "also known as" names, addresses, and phonetic spelling of names were also used. When there was a discrepancy in cancer diagnosis dates between registries, the first report of a given cancer was chosen. Because cancer registry reporting of basal and squamous cell skin cancers, recurrent cancers, and in situ cervical cancers is not required by law, these were excluded from the analyses. We also excluded in situ anogenital cancers because they are considered precancerous and noninvasive.
To minimize the possibility that a cancer occurred prior to HIV infection, in this analysis we included only those cancers that occurred within 5 years before the initial AIDS diagnosis or anytime thereafter, as has been done in previous registry linkage studies (7–13). This 5-year window also reduces the likelihood of missing a cancer diagnosed outside of California, in the case of inward migration.
The characteristics considered in this analysis included demographic factors (age, race/ethnicity, sex), HIV risk group, year of cancer diagnosis, HAART use, calendar year, stage and grade of cancer at diagnosis, and cancer treatment. The California Cancer Registry collects information on all cancer treatment given or planned within 4 months after diagnosis, including surgery, radiation, and chemotherapy. All cancer treatments recorded in the California Cancer Registry were considered; if any treatment was indicated, we then coded that person as cancer treated. If all the treatment variables were recorded as no, we then coded that person as untreated. For the remainder, cancer treatment was considered unknown. We characterized the study sample by date of AIDS diagnosis using standard descriptive statistics. Multiple incident cancers were included, and the data were censored at date of death, loss to follow-up, or December 31, 2003, whichever occurred first.
Each cancer was classified by using the Surveillance, Epidemiology, and End Results (SEER) Program site recoding scheme, which is based on the International Classification of Diseases for Oncology, Second Edition and International Classification of Diseases for Oncology, Third Edition, with Kaposi's sarcoma and mesothelioma definitions added to the cancer categories (14). To determine whether there was an excess cancer incidence for cancers types that occurred in one or more persons, we compared the cancer site-specific rates for the AIDS cases with those for adults from the San Francisco, California, population-based SEER (14). The expected numbers of cancers were computed by using sex-, race-, and age-specific rates from the San Francisco SEER registry from January 1, 1985, through December 31, 2001, the most recent year available from SEER at the time of this analysis.
Persons whose cancer was diagnosed prior to their AIDS diagnosis had to live long enough to develop AIDS. Thus, the estimates of expected cancers needed to be adjusted downward to account for patients with cancer who died before developing AIDS. We applied cancer survival rates for specific malignancies to calculate survival-conditioned cancer incidence rates covering each year up to 5 years before AIDS onset (14). For a yearly interval such as 1 year before AIDS onset (midpoint, 6 months before AIDS onset), we used the 6-month survival rate for specific malignancies to estimate the proportion of persons diagnosed with cancer who would be alive 6 months later. These rates were divided in strata of sex, race, and 5-year age groups and were multiplied by the appropriate pre-AIDS person-years of observation. The products were summed to yield the expected number of cancers. Standardized incidence ratios (SIRs), adjusted for age (5-year categories), sex, and race (White, Black, other), were calculated by using indirect standardization (15).
We also considered misclassification of certain cancers and checked whether any of the nonepithelial skin or soft tissue cases of cancer from the cancer registry were listed as Kaposi's sarcoma in the AIDS registry. From the cancer registry database, we identified two persons with nonepithelial skin cancers and another two with soft tissue cancer who, according to the AIDS registry, also had Kaposi's sarcoma. However, the dates of non-AIDS cancer diagnosis and histologic description of the cancers were quite different from the Kaposi's sarcoma information. We therefore included these cancers in our calculation of the nonepithelial skin and soft tissue SIRs. Similarly, we checked whether any of the brain or other nervous system cases of cancer from the cancer registry were listed as non-Hodgkin's lymphoma in the AIDS registry. We found one person listed in the cancer registry with brain or other nervous system cancer who was also listed in the AIDS registry with central nervous system non-Hodgkin's lymphoma. Again, the date of the non-AIDS cancer diagnosis and histologic description of the cancer were very different from the non-Hodgkin's lymphoma information, and this case was included when we calculated the brain or other nervous system SIR.
To evaluate the effect of HAART use on risk of cancer, unadjusted and adjusted Cox proportional hazards models were performed with time zero being 5 years before AIDS diagnosis and HAART treated as a time-varying covariate. Adjusted models considered calendar year and HAART era (January 1, 1996, or later) as a time-varying covariate, age at AIDS diagnosis, race (Whites as the reference group), risk group (other risk as the reference group), and sex (males as the reference group).
For the three most common cancers, we performed cancer-specific unadjusted and adjusted Cox proportional hazards analyses to evaluate factors associated with cancer survival time. The survival models were corrected for late entry because those who died before being diagnosed with AIDS could not be included in this study. HAART use was defined as a three-category time-varying covariate that took into account both the availability of HAART and amount of HAART use. These categories were 1) no HAART use (the reference group), 2) <6 months of HAART use, and 3) 
6 months of HAART use. We also created three calendar-time categories: 1990–1995 (pre-HAART), 1996–1999 (early HAART era), and 2000–2003 (recent HAART era). In the adjusted models, we retained year of cancer diagnosis and the time-varying HAART use and calendar-time indicator variables. We then used backward elimination and retained only those other factors associated with cancer survival at the p < 0.10 level. Survival time was calculated from date of cancer diagnosis to date of death or, if alive, was censored at December 31, 2003. The proportionality assumption was evaluated both statistically and graphically and appeared to be satisfied for all the models. All statistical analyses were performed by using SAS software (16).
The Committee on Human Research at the University of California, San Francisco, reviewed and approved of the study protocol.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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A total of 17,709 adult AIDS cases were matched with the California Cancer Registry. We subsequently excluded 2,080 cases who were non–San Francisco residents at the time of their initial AIDS diagnosis. Another 1,389 patients were excluded who had no information on HAART use and were lost to follow-up during the HAART time period (after January 1, 1996). We also excluded 22 cancers that were coded as ill defined or unspecified since there was no way to determine whether they were AIDS-defining cancers. Finally, eight cases were excluded because they had a non-AIDS cancer diagnosed more than 60 months prior to their initial AIDS diagnosis. These eight cancers were one of each of the following: anal, Hodgkin's disease, melanoma, prostate, renal/pelvis, brain, thyroid, and nonepithelial skin.
Our final analytic sample included 14,210 adults who were diagnosed with AIDS and resided in San Francisco at the time of their initial AIDS diagnosis during the period January 1, 1990, through December 31, 2000. Of these 14,210 adults, 4,331 (30.5 percent) had a cancer diagnosis 5 years prior to or at or after the time of their initial AIDS diagnosis. Table 1 provides patient characteristics by time period of AIDS diagnosis, prior to or after the availability of HAART, and by HAART status for those diagnosed with AIDS in the HAART era. Compared with those diagnosed with AIDS prior to January 1, 1996, those diagnosed with AIDS in the HAART era were older, more likely to be non-White, less likely to be men who have sex with men, more likely to have a CD4 cell count of <200 at AIDS diagnosis, and less likely to have an AIDS-related cancer (p < 0.001). Among only those diagnosed with AIDS on or after January 1, 1996, those receiving HAART for at least 6 months prior to their diagnosis were more likely to be White, be male, have CD4 cell counts of >350, and be less likely to have an AIDS-related cancer compared with those with little or no HAART use (p < 0.05). The proportion with non-AIDS-related cancers was similar in all three groups.
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A total of 482 non-AIDS-defining cancers were diagnosed, 156 at the time of or up to 5 years before AIDS diagnosis and 326 subsequent to AIDS diagnosis. The most common non-AIDS cancers were respiratory (n = 86), anal (n = 79), Hodgkin's lymphoma (n = 69), oral cavity and pharynx (n = 37), melanoma (n = 36), prostate (n = 32), liver (n = 23), testis (n = 16), and leukemia (n = 15).
Cancer incidence
Compared with the SEER cancer rates, the crude rate revealed an excess for all non-AIDS cancers combined, as well as the following specific cancer types: oral cavity and pharynx, anal, liver, respiratory, melanoma, and Hodgkin's disease (table 2). After adjustment for differential survival, the rates of these cancers as well as prostate cancer and leukemia were found to be higher than expected: all non-AIDS cancers (SIR = 2.3), oral cavity and pharynx (SIR = 2.6), anal (SIR = 13.4), liver (SIR = 3.6), respiratory (SIR = 2.6), melanoma (SIR = 2.4), prostate (SIR = 1.7), Hodgkin's disease (SIR = 11.5), and leukemia (SIR = 2.4).
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The risk of developing a non-AIDS cancer was slightly higher in the HAART era (relative hazard (RH) = 1.43) and slightly lower for those who used HAART (RH = 0.79, table 3). After adjustment for age at AIDS diagnosis, race, risk group, sex, calendar year, HAART use, and HAART era, the risk of anal cancer was statistically significantly higher in the HAART era (RH = 2.74). When the analysis was restricted to men who have sex with men only, the risk was slightly higher (RH = 2.93). The adjusted risk for liver cancer was statistically significantly lower with HAART use (RH = 0.32). For several other cancers, the estimated HAART effects were of similar or greater magnitude, some in the direction of risk, but did not reach statistical significance.
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Cancer survival time
Tables 4–6 show the relative hazards from the unadjusted and adjusted proportional hazards survival analyses. In the adjusted model for anal cancer (table 4), distant stage of disease (RH = 5.18) was associated with shorter cancer survival, and cancer treatment (RH = 0.04) was associated with longer survival. For respiratory cancer (table 5), distant stage of disease (RH = 2.96) was associated with a shorter survival time, while at least 6 months of HAART use (RH = 0.40) and cancer treatment (RH = 0.44) were associated with a longer survival time. For Hodgkin's lymphoma (table 6), older age at cancer diagnosis (RH = 1.67), lymphocyte depletion (RH = 37.32), and not-otherwise-specified histology (RH = 3.70) were associated with shorter cancer survival, while 6 months or more of HAART use (RH = 0.17) was associated with increased survival time.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Several studies have linked HIV/AIDS registries with cancer registries to assess the risk of cancer for persons with HIV and AIDS. However, to our knowledge, none of these studies have had direct measures of HAART use by registry patients. Instead, they have assessed calendar period (pre-HAART era to HAART era) to indirectly measure the potential effect of HAART on cancer incidence. Ours is one of the first studies, if not the first, to incorporate data on antiretroviral use with the information on cancer and AIDS incidence and cancer survival time.
Although HAART was estimated to have substantial impacts, both increases and decreases, on the risks of many types of non-AIDS-defining cancers, most estimates had very wide confidence intervals. Living during the HAART era appeared to confer a slightly higher risk of developing a non-AIDS cancer (p = 0.060) and a significantly higher risk of developing anal cancer (p = 0.044 for all risk groups and p = 0.033 for men who have sex with men only). The increased risk for all non-AIDS cancers combined in the HAART era is likely due to a reduction in the AIDS-related causes of morbidity and mortality. The increased risk of developing anal cancer may also be due to more frequent screening or better surveillance of disease in the HAART era or to longer life expectancy among those with persistent human papillomavirus infection. The increased risk is not likely due to earlier detection since anal cancer survival is significantly shorter for the same time period. Interestingly, although the overall incidence of liver cancer was higher than expected in the general population, in the proportional hazards analysis, the incidence was significantly lower with HAART use compared with no HAART use (p = 0.025). This finding implies that the higher-than-expected rate of liver cancer may be due to factors, such as coinfection with hepatitis B or C viruses, other than HAART-related hepatotoxicity.
In the multivariate proportional hazards models of cancer survival time, respiratory cancer and Hodgkin's lymphoma showed an association with at least 6 months of HAART use and longer cancer survival time. Anal cancer survival time was affected by two contributory phenomena: an apparent increased hazard for the HAART era (especially in 1996–1999) and an increased hazard for those with more than 5 months of HAART use. The adjusted survival time analyses also highlighted other factors, such as cancer treatment and type of cancer at presentation, that influenced cancer survival time. Patients who did not receive cancer treatment may also have been sicker or have had more advanced cancer than the patients who received such treatment; thus, we cannot fully attribute longer survival time to treatment per se. In addition, those persons receiving HAART and who receive cancer treatment may have better access to health care than those not receiving treatment, and this difference may lead to longer survival time.
Previous studies have reported HAART-related (measured either directly or by way of calendar time) improved survival after a non-AIDS-defining cancer diagnosis in persons with HIV/AIDS. Improved postcancer survival was found for Hodgkin's lymphoma in at least three studies (17–19) and for colorectal, anal, and female breast cancer in at least one other study (19). On the other hand, a few studies have not found any change in survival for anal cancer (20) or lung cancer (21), which might be due to insufficient follow-up time or use of calendar time as a surrogate measure for HAART use. Disentangling the effect of HAART from the effect of cancer treatment is difficult, especially since both HIV and cancer treatments have improved in recent years and patients may be more likely to undergo cancer treatment given the longer life expectancy in the HAART era.
The clinical management of malignancies in HIV-infected persons is also evolving and will likely result in improved cancer survival time. The feasibility and toxicity, including drug-drug interactions, of using the combination of HAART and chemotherapy is an important consideration. Yet, most of the treatment strategies now recommend continuing HAART during cancer treatments, including chemotherapy, until unacceptable toxicity occurs. By possibly limiting immune damage inflicted by HIV, HAART administration during chemotherapy may even enable the development of antitumor responses, thereby reducing HIV-associated production of proinflammatory cytokines (4).
In our analyses that did not incorporate HAART use, we observed an excess risk of oral cavity and pharynx, anal, liver, and respiratory cancer; melanoma; prostate cancer; Hodgkin's disease; and leukemia among persons with HIV and AIDS. Compared with those from other studies that linked AIDS and cancer registries, our results are similar for cancers of the oral cavity and pharynx (9, 10, 22), anus (8, 11, 12, 22), and respiratory system (9, 10, 13, 22), and for Hodgkin's disease (9–12, 22). We also found an excess of liver cancer, melanoma of the skin, prostate cancer, and leukemia, which have been postulated as being elevated in people with AIDS but have not been consistently reported as such (9–12, 22).
Also of interest are the cancers not seen in excess, including stomach, small intestine, colon, breast, bladder, and thyroid. This finding is also in accord with results from other studies that have evaluated the risk of cancer for persons with HIV/AIDS (9, 10, 12, 22, 23). This finding demonstrates that the effect of HIV infection on tumorigenesis is variable and that the cancers found to be in excess among persons with HIV and AIDS are those more likely to have a viral agent associated with their pathology (24).
Our findings are not without limitations. First, several of the non-AIDS cancers occurred very infrequently; therefore, our sample size was not sufficient to reach definitive conclusions. However, we observed 482 non-AIDS cancers in the 14,210 adults with AIDS and produced useful estimates of the risk of many non-AIDS cancers. Another limitation of our data was the lack of information on cigarette smoking, which may be responsible for the observed excess risk of certain cancers such as those of the respiratory system, and oncogenic viral infections, such as human papillomavirus, which is the likely cause of most anogenital cancers. In addition, our determination of HAART use depended on medical chart abstraction, and HAART may have been underreported for some cases or misclassified, and our determination of cancer treatment was ascertained from the cancer registry and may be incomplete. In addition, the follow-up time for those initially diagnosed with AIDS in 1998–2000 is relatively short. Lastly, other temporal effects may have contributed to a change in incidence or survival of non-AIDS cancer cases in the era of HAART that we did not consider in our analyses. For example, improvements in cancer prevention, screening, or treatment may be responsible for observed decreases or increases in cancer incidence or cancer survival time. However, by including calendar year and year of cancer diagnosis in our analyses, we were able to indirectly adjust for temporal changes in cancer diagnoses and treatment.
In summary, HAART use does not appear to substantially reduce non-AIDS cancer risk overall, and the impact of HAART on specific non-AIDS-defining cancer incidence rates and survival time is not uniform, with cancer incidence rates and survival time changing for some but not all cancers. The underlying etiology for each cancer type contributes to this observed variation, along with changes in HIV and cancer treatments. Appropriate cancer prevention, screening, and treatment efforts are necessary, along with a better understanding of the etiology, epidemiology, and natural history of AIDS and non-AIDS-defining malignancies.
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ACKNOWLEDGMENTS |
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The National Institute of Allergy and Infectious Diseases funded this project under grant RO3-AI055270. The authors are grateful for funding for San Francisco AIDS surveillance from the Centers for Disease Control and Prevention, grant U62/CCU923549-03.
The authors acknowledge the assistance of David Harris at the California Cancer Registry and Jennie Chin at the San Francisco Public Health Department HIV/AIDS Statistics, Epidemiology and Intervention Research Branch.
Conflict of interest: none declared.
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